The effect of melatonin on mitochondrial function in endotoxemia induced by lipopolysaccharide

Asian-Australasian Journal of Animal Sciences

Volumn 24, Issue 6, 2011, Pages 857-866

  Liu, Jing ^a   Wu, Fengming ^a   Liu, Yuqing ^a   Zhang, Tao ^a   Tang, Zhaoxin ^a  

^a SOUTH CHINA AGRICULTURAL UNIVERSITY   (China)

Author keywords

Endotoxemia; Free radicals; Goat; Melatonin; Mitochondrial function

Indexed keywords

CAPRA HIRCUS;

EID: 79960226694     PISSN: 10112367     EISSN: None     Source Type: Journal    
DOI: 10.5713/ajas.2011.10180     Document Type: Article

References (73)

1. Acuna-Castroviejo, D., G. Escames, J. Leon, A. Carozo and H. Khaldy. 2003. Mitochondrial regulation by melatonin and its metabolites. Adv. Exp. Med. Biol. 527:549-557. (Pubitemid 38197684)
2. Acuna-Castroviejo, D., M. Martin, M. Macias, G. Escames, J. Leon, H. Khaldy and R. J. Reiter. 2001. Melatonin, mitochondria, and cellular bioenergetics. J. Pineal Res. 30:65-74. (Pubitemid 32176208)
3. Allegra, M., R. J. Reiter, D. X. Tan, C. Gentile, L. Tesoriere and M. A. Livrea. 2003. The chemistry of melatonin's interaction with reactive species. J. Pineal Res. 34:1-10. (Pubitemid 36140351)
4. Anatoly, A. S. and F. Gary. 2003. Regulation of brain mitochondrial H2O2 production by membrane potential and NAD(P)H redox state. J. Neurochem. 86:1101-1107.
5. Andrey, V. K., S. Katrin and H. Susanne. 2006. Different effects of endotoxic shock on the respiratory function of liver and heart mitochondria in rats. Am. J. Physiol. Gastrointest. Liver Physol. 290:543-549.
6. Andreyev, A. Yu, Kushnareva Yu. E. and A. A. Starkov. 2005. Mitochondrial metabolism of reactive oxygen species. Biochem. (Moscow) 70:200-214. (Pubitemid 40512329)
7. Aydogen, S., M. B. Yerer and A. Goktas. 2006. Melatonin and nitric oxide. J. Endocrinol. Invest. 29:281-287.
8. Barja, G. 1999. Mitochondrial oxygen radicals generation and leak: sites of production in states 4 and 3, organ specificity, and relation to aging and longevity. J. Bios. Bioe. 31:347-366. (Pubitemid 30058570)
9. Bass, D. A., J. W. Parce, L. R. Dechatelet, P. Szejda, M. C. Seeds and M. Thomas M. 1983. Flow cytometric studies of oxidative product formation by neutrophils: A graded response to membrane stimulation. J. Immunol. 130:1910-1915.
10. Bettahi, I., J. M. Guerrero, R. J. Reiter and C. Osuna. 1998. Physiological concentrations of melatonin inhibit the norepinephrineinduced activation of prostaglandin E2 and cyclic AMP production in rat hypothalamus: a mechanism involving inhibiton of nitric oxide synthase. J. Pineal Res. 25: 34-40.
11. Bi, M. H., S. W. Zhang and B. E. Wang. 2004. The impairment and mechanism of endotoxemia in rat liver mitochondria. J. Chi. Integ. Med. 20:90-91.
12. Brealey, D., M. Brand, I. Hargreaves, S. Heales, J. Land, R. Smolenski, N. A. Davies, C. E. Cooper and M. Singer. 2002. Association between mitochondrial dysfunction and severity and outcome of septic shock. Lancet 360:9-223.
13. Cawthon, D. C., R. McNew, K. W. Beers and W. G. Bottje. 1999. Evidence of mitochondrial dysfunction in broilers with pulmonary hypertension syndrome (ascites): Effect of t-butyl hydroperoxide on hepatic mitochondrial function, glutathione, and related thiols. Poult. Sci. 78:114-124. (Pubitemid 129554730)
14. Costa, E. J., C. S. Shida, M. H. Biaggi, A. S. Ito, M. T. Lamy-Freund. 1997. How melatonin interacts with lipid bilayers: a study by fluorescence and ESR spectroscopies. FEBS Lett. 416: 103-106. (Pubitemid 27470811)
15. Crespo, E., M. Macias, D. Pozo, G. Escames, M. Martin, F. Vives, J. M. Guerrero and D. Acuna-Castroviejo. 1999. Melatonin inhibits expression of the inducible NO synthase II in liver and lung and prevents endotoxemia in lipopolysaccharideinduced multiple organ dysfunction syndrome in rats. FASEB J. 13: 1537-1546. (Pubitemid 29411787)
16. Crouser, E. D. 2004. Mitochondrial dysfunction in septic shock and multiple organ dysfunction syndrome. Mitochondrion 4: 729-741. (Pubitemid 39646818)
17. Crouser, E. D., M. W. Julian, D. V. Blaho and D. R. Pfeiffer. 2002. Endotoxin-induced mitochondrial damage correlates with impaired respiratory activity. Crit. Care Med. 30:276-284. (Pubitemid 34158107)
18. Crouser, E. D., M. W. Julian and P. M. Dorinsky. 1999. Ileal VO2-DO2 alterations induced by endotoxin correlate with severity of mitochondrial injury. Am. J. Respir. Crit. Care Med. 160: 1347-1353. (Pubitemid 29487479)
19. Elizabeth, A. M. and F. A. Karam. 2004. Effects of enhancing mitochondrial oxidative phosphorylation with reducing equivalents and ubiquinone on 1-methyl-4-phenylpyridinium toxicity and complex I-IV damage in neuroblastoma cells. Biomed. Pharmacother. 67:1167-1184.
20. Escames, G., J. Leon, M. Macias, H. Khaldy and D. Acuna-Castroviejo. 2003. Melatonin counteracts lipopolysaccharideinduced expression and activity of mitochondrial nitric oxide synthase in rats. FASEB J. 17:932-934.
21. Fink, M. P. 2001. Cytopathic hypoxia: mitochondrial dysfunction as mechanism contributing to organ dysfunction in sepsis. Crit. Care Clin. 17:219-237. (Pubitemid 32163188)
22. Francesca, P., T. Jukka and W. Christian. 2006. Effects of prolonged endotoxemia on liver, skeletal muscle and kidney mitochondrial function. Crit. Care 10:118-130.
23. Galente, Y. M. and Y. Hatefi. 1978. Resolution of Complex I and isolation of NADH dehydrogenase and an iron-sulfur protein. Meth. Enzymol. 53:15-21.
24. Garcia, J. J., R. J. Reiter, J. Pie, G. G. Ortiz, J. Cabrera, R. M. Sainz and D. Acuna-Castroviejo. 1999. Role of pinoline and melatonin in stabilizing hepatic microsomal membranes against oxidative stress. J. Bioenerg. Biomembr. 31:609-616. (Pubitemid 30082903)
25. Giuseppe, P. M.P.a.F.M.R. 2000. The effect of reactive oxygen species generated from the mitochondrial electron transport chain on the cytochrome c oxidase activity and on the cardiolipin content in bovine heart submitochondrial particles. FEBS Lett. 466:323-326.
26. Haider R., J. Annie, M. B. Eric, B. Sheela and K. Amr. 2006. Alterations in mitochondrial respiratory functions, redox metabolism and apoptosis by oxidant 4-hydroxynonenal and antioxidants curcumin and melatonin in PC 12 cells. Toxicol. Appl. Pharmacol. 226:161-168.
27. Hartmut, J., J. G. Gregory, I. C. Arthur, A. H. Jack, P. Dominique and J. L. John. 2002. Mech Hepatotox. Toxicol. Sci. 65:166-176.
28. Hatefi, Y. and D. L. Stiggall. 1978. Preparation and properties of succinate: ubiquinone reductase (Complex II). Meth. Enzymol. 53: 21-27.
29. Hiroyuki, T. 2006. Mitochondrial oxidative stress and heart failure. Inter. Med. 45:809-813.
30. Iqbal, M., D. Cawthon, R. F. Widenman, Jr., K. W. Beers and W. G. Bottje. 2001a. Lung mitochondrial dysfunction in pulmonary hypertension syndrome. II. Oxidative stress and inability to improve function with repeated additions of ADP. Poult. Sci. 80:656-665. (Pubitemid 33659946)
31. Jane, A. L. and L. Joseph. 2005. Oxidative enzymopathies and vascular disease. Arterioscler. Thromb. Vas. Biol. 25:1102-1111.
32. Kantrow, S. P., D. E. Taylor, M. S. Carraway and C. A. Piantadosi. 1997. Oxidative metabolism in rat hepatocytes and mitochondria during sepsis. Arch. Biochem. Biophys. 345:278-288. (Pubitemid 27400621)
33. Kubes, P. 2005. The complexities of leukocyte recruitment. Semin. Immuno. 14:65-72.
34. Leon, J., D. Acuna-Castroviejo, G. Escames, D. X. Tan and R. J. Reiter. 2005. Melatonin mitigates mitochondrial malfunction. J. Pineal Res. 38:1-9. (Pubitemid 40139304)
35. Leon, J., M. Macias, G. Escames, E. Camacho, H. Khaldy, M. Martin, A. Espinosa, M. A. Gallo and D. Acuna-Castroviejo. 2000. Structure-related inhibition of calmodulin-dependent neuronal nitric-oxide synthase activity by melatonin and synthetic kynurenines. Mol. Pharm. 58:967-975
36. Leon, J., F. Vives, E. Crespo, E. Camacho, A. Espinosa, M. A. Gallo, G. Escames and D. Acuna-Castroviejo. 1998. Modification of nitric oxide synthase activity and neuronal response in rat striatum by melatonin and kynurenine derivatives. J. Neuroendocrinol. 10:297-302. (Pubitemid 28177351)
37. Lobo, S. M., D. De Backer, Q. Sun, Z. Tu, G. Dimopoulos, J. C. Preiser, N. Nagy, B. Vray, V. Vercrury, R. G. Terzi and J. L. Vincent. 2003. Gut mucosal damage during endotoxic shock is due to mechanisms other than gut ischemia. J. Appl. Phys. 95:2047-2054. (Pubitemid 37314003)
38. Lothar, K. and H. Judy. 2006. The mechanism of superoxide production by NADH: ubiquinone oxidoreductase (complex I) from bovine heart mitochondria. Proc. Nat. Ac. Sci. 103:7607-7612.
39. Lu, S. M., S. M. Song, J. C. Liu, H. M. Yang, P. Li and Z. G. Wang. 2003. Changes of proton transportation across the inner mitochondrial membrane and H-ATPase in endotoxic shock rats. Chin. J. Traumatol. 6:292-296. (Pubitemid 37236340)
40. Ly, J. D., D. R. Grubb, and A. Lawen. 2003. The mitochondrial membrane potential [Deltapsi(m)] in apoptosis: an update. Apoptosis 8:115-118.
41. Marieke, K. B. V. D. W. and Emile De Heer. 1996. Cisplatininduced nephrotoxicity in porcine proximal tubular cells: Mitochondrial dysfunction by inhibition of complexes I to IV of the respiratory chain. J. Pharmacol. Exp. Ther. 280:638-649.
42. Marion, M. B. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:248-254.
43. Martinez, G. R., E. A. Almeida, C. F. Klitzke, J. Onuki, F. M. Prado, M. H. Medeiros and P. Di Mascio. 2005. Measurement of melatonin and its metabolites: importance for the evaluation of their biological roles. Endocrine 27:111-118. (Pubitemid 41558443)
44. Matthew, M., L. Michael, R. T. David and T. R. Michael. 2006. Mitochondrial respiratory chain supercomplexes are destabilized in barth syndrome patients. J. Mol. Biol. 261:462-469.
45. Menendez-Pelaez, A. and R. J. Reiter. 1993. Distribution of melatonin in mammalian tissues: the relative importance of nuclear versus cytosolic localization. J. Pineal Res. 15:59-69. (Pubitemid 24028611)
46. Michael, R. D. 2000. Mitochondria and calcium: from cell signaling to cell death. J. Phys. 529:57-68.
47. Michael, R. D. 2004. Section III: mitochondria, β-cell function, and type 2 diabetes. Role of mitochondria in health and disease. Diabetes 53:S96-S102.
48. Octavio, G., A. Angeles, M. Lourdes and P. B. Juan. 2005. Increased mitochondrial respiration maintains the mitochondrial membrane potential and promotes survival of cerebellar neurons in an endogenous model of glutamate receptor activation. J. Neurochem. 92:183-190.
49. Ojano-Dirain, C., M. Iqbal, T. Wing, M. Cooper and W. Bottje. 2005. Glutathione and respiratory chain complex activity in duodenal mitonchondria of broilers with low and high feed efficiency. Poult. Sci. 84:785-788.
50. Pozo, D., R. J. Reiter, J. R. Calvo and J. M. Guerrero. 1994. Physiological concentrations of melatonin inhibit nitric oxide synthase in rat cerebellum. Life Sci. 55:PL455-PL460. (Pubitemid 24347808)
51. Qun, C., J. V. Edwin, M. Shadi and L. H. Charles. 2003. Production of reactive oxygen species by mitochondria: Central role of complex III. J. Biol. Chem. 278:36027-36031.
52. Raam, B. J., S. Wim, W. de Elly, R. Dirk, J. V. Arthur and W. K. Taco. 2008. Mitochondrial membrane potential in human neutrophils is maintained by complex III activity in the absence of supercomplex organization. PLoS ONE 3:e2013.
53. Reiter, R. J., D. X. Tan, L. C. Manchester and W. Qi. 2001a. Biochemical reactivity of melatonin with reactive oxygen and nitrogen species. Cel. Physiol. Biochem. 34:237-256. (Pubitemid 33615836)
54. Reiter, R. J., D. X. Tan and C. Osuna. 2000. Actions of melatonin in the reduction of oxidative stress: a review. J. Biomed. Sci. 7: 444-458.
55. Reiter, R. J., D. X. Tan, L. C. Manchester and M. R. El-Sawi. 2002. Melatonin reduces oxidant damage and promotes mitochondrial respiration: implications for aging. Ann. NY Acad. Sci. 959:238-250. (Pubitemid 34457565)
56. Rodriquez, C., J. C. Mayo and R. J. Saina. 2004. Regulation of antioxidant enzymes: a significant role for melatonin. J. Pineal Res. 36:1-9. (Pubitemid 38130283)
57. Rongen, G. A., P. Smits and T. Thien. 1994. Endothelium and the regulation of vascular tone with emphasis on the role of nitric oxide. Physiology, pathophysiology and clinical implications. Neth. J. Med. 44:26-35. (Pubitemid 24066554)
58. Shauna, M. D. and K. Aly. 2006. Lipopolysaccharide signaling in endothelial cells. Lab. Invest. 86:9-22.
59. Singer, M. and D. Brealey. 1999. Mitochondrial dysfunction in sepsis. Biochem. Soc. Symp. 66:149-166. (Pubitemid 129639030)
60. Singer, M., V. De Santis, D. Vitale and W. Jeffcoate. 2004. Multiorgan failure is an adaptive, endocrine-mediated, metabolic response to overwhelming systemic inflammation. Lancet 364:545-548. (Pubitemid 39070417)
61. Tan, D. X., L. D. Chen and B. Poeggeler. 1993. Melatonin: a potent, endogenous hydroxyl radical scavenger. Endocr. J. 1: 57-60.
62. Tan, D. X., L. C. Manchester, R. J. Reiter, B. F. Plummer, J. Limson, S. T. Weintraub and W. Qi. 2000a. Melatonin directly scavenges hydrogen peroxide: a potentially new metabolic pathway of melatonin. Free Radic. Biol. Med. 29:1177-1185.
63. Tan, D. X., L. D. Chen, B. Poeggeler, L. C. Manchester and R. J. Reiter. 1993a. Melatonin: a potent endogenous hydroxyl radical scavenger. Endocr. J. 1:57-60.
64. Tan, D. X., B. Poeggeler, R. J. Reiter, L. D. Chen, S. Chen, L. C. Manchester and L. R. Barlow-Walden. 1993b. The pineal hormone melatonin inhibits DNA-adduct formation induced by the chemical carcinogen safrole in vivo. Cancer Lett. 70:65-71. (Pubitemid 23219861)
65. Tang, Z., M. Iqbal and D. Cawthon. 2002. Heart and breast muscle mitochondrial dysfunction in pulmonary hypertension syndrome in broilers (gallus domesticus). Comp. Biochem. Physiol. Part A 132:527-540. (Pubitemid 34607311)
66. Tatyana, V. V. and J. R. Ian. 2001. Δψm-Dependent and-independent production of reactive oxygen species by rat brain mitochondria. J. Neurochem. 79:266-277.
67. Tsutsui, H. 2006. Mitochondrial oxidative stress and heart failure. Jap. Soc. Inter. Med. 45:809-813. (Pubitemid 44194346)
68. Turrens, J. F. 1997. Superoxie production by the mitochondrial respiratory chain. Biosci. Rep. 17:3-8. (Pubitemid 27267586)
69. Vera, A. V. and C. Christos. 2006. Bioenergetics and the formation of mitochondrial reactive oxygen species. Trends Pharmacol. Sci. 27:639-645.
70. Wang, Y. L., S. Zhang and Z. X. Tang. 2006. Effect of ainoguanidine on liver mitochondrial free radical metabolism in broilers with endotoxemia. Chin. J. Vet. Sci. 36:143-146.
71. Wu, K. K. and P. Thiagarajan. 1996. Role of endothelium in thrombosis and hemostasis. Annu. Rev. Med. 47:315-331. (Pubitemid 26138894)
72. Ximenes, V. F., S. O. Silva, M. R. Rodrigues, L. H. Catalani, G. J. Maghzal, A. J. Kettle and A. Campa. 2005. Superoxide dependent oxidation of melatonin by myeloperoxidase. J. Biol. Chem. 280:38160-38169. (Pubitemid 43853710)
73. Zavodnik, I. B., E. A. Lapshima, L. B. Zavodnik, M. Labieniec, M. Bryszewska and R. J. Reiter. 2004. Hypochlorous acidinduced oxidative stress in Chinese hamster B14 cells: viability, DNA and protein damage and the protective action of melatonin. Mutat. Res. 559:39-48. (Pubitemid 38452916)